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Regulation of the Serotonergic System by Kainate in the Avian Retina

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Abstract

Serotonin (5-HT) has been recognized as a neurotransmitter in the vertebrate retina, restricted mainly to amacrine and bipolar cells. It is involved with synaptic processing and possibly as a mitogenic factor. We confirm that chick retina amacrine and bipolar cells are, respectively, heavily and faintly immunolabeled for 5-HT. Amacrine serotonergic cells also co-express tyrosine hydroxylase (TH), a marker of dopaminergic cells in the retina. Previous reports demonstrated that serotonin transport can be modulated by neurotransmitter receptor activation. As 5-HT is diffusely released as a neuromodulator and co-localized with other transmitters, we evaluated if 5-HT uptake or release is modulated by several mediators in the avian retina. The role of different glutamate receptors on serotonin transport and release in vitro and in vivo was also studied. We show that l-glutamate induces an inhibitory effect on [3H]5-HT uptake and this effect was specific to kainate receptor activation. Kainate-induced decrease in [3H]5-HT uptake was blocked by CNQX, an AMPA/kainate receptor antagonist, but not by MK-801, a NMDA receptor antagonist. [3H]5-HT uptake was not observed in the presence of AMPA, thus suggesting that the decrease in serotonin uptake is mediated by kainate. 5-HT (10–50 μM) had no intrinsic activity in raising intracellular Ca2+, but addition of 10 μM 5-HT decreased Ca2+ shifts induced by KCl in retinal neurons. Moreover, kainate decreased the number of bipolar and amacrine cells labeled to serotonin in chick retina. In conclusion, our data suggest a highly selective effect of kainate receptors in the regulation of serotonin functions in the retinal cells.

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Acknowledgments

Grants from Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Instituto Nacional de Ciência e Tecnologia de Neurociência Translacional (INCT-INNT), Instituto Nacional de Ciência e Tecnologia de Neuroimodulação (INCT-NIM), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) supported this work. DPF thanks CAPES/Brazil for doctoral fellowships. JLMN and AMH thank CNPQ for the individual research fellowship. KCC and RAMR thank CNPq and FAPERJ for the individual research fellowship. We thank Granja Americano (Santa Izabel Alimento LTDA) for kindly providing Fertilized White Leghorn eggs (Gallus gallus) for our experiments.

Funding

This study was funded by CNPq (Grant number 552491/2011-0).

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Authors and Affiliations

  1. Laboratório de Neuroquímica Molecular e Celular, Instituto de Ciências Biológicas, Universidade Federal do Pará, Campus Universitário do Guamá, Rua Augusto Correa 01, Belém-PA, 66075-110, Brazil

    Adelaide da Conceição Fonseca Passos, Anderson Manoel Herculano, Karen R. H. M. Oliveira & José Luiz Martins do Nascimento

  2. Lab de Neurobiologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém-PA, Brazil

    Silene Maria A. de Lima & Fernando A. F. Rocha

  3. Laboratório de Neuroquímica, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio De Janeiro-RJ, Brazil

    Hércules Rezende Freitas, Luzia da Silva Sampaio, Danniel Pereira Figueiredo & Ricardo Augusto de Melo Reis

  4. Escola de Ciências da Saúde, Centro Universitário IBMR, Rio De Janeiro-RJ, Brazil

    Hércules Rezende Freitas

  5. Lab Neurobiologia da Retina, Programa de Pós-graduação em Neurociências, Universidade Federal Fluminense, Rio De Janeiro-RJ, Brazil

    Karin da Costa Calaza

Authors
  1. Adelaide da Conceição Fonseca Passos
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  2. Anderson Manoel Herculano
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  3. Karen R. H. M. Oliveira
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  4. Silene Maria A. de Lima
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  5. Fernando A. F. Rocha
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  6. Hércules Rezende Freitas
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  7. Luzia da Silva Sampaio
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  8. Danniel Pereira Figueiredo
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  9. Karin da Costa Calaza
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  10. Ricardo Augusto de Melo Reis
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  11. José Luiz Martins do Nascimento
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Contributions

Conceived and designed the experiments: LSS, HRF, KCC, RAMR, and JLMN. Performed the experiments: ACFP, SMAL, LSS, HRF, FAFR, and DPF. Analyzed the data: AMH, KRHMO, KCC, RAMR, and JLMN. Contributed reagents/materials/analysis tools: KCC, RAMR, and JLMN. Wrote the paper and financial support and administrative support: KCC, RAMR, and JLMN.

Corresponding author

Correspondence to José Luiz Martins do Nascimento.

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The authors declare that they have no conflict of interest.

Ethical Approval

All experiments involving animals were approved and carried out in accordance with the guidelines of the Institutional Animal Care and Use Committee of the Federal University of Pará (permit number 85/15) and Federal University of Rio de Janeiro (permit number IBCCF-035).

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Passos, A.d., Herculano, A.M., Oliveira, K.R.H.M. et al. Regulation of the Serotonergic System by Kainate in the Avian Retina. Cell Mol Neurobiol 39, 1039–1049 (2019). https://doi.org/10.1007/s10571-019-00701-8

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  • DOI: https://doi.org/10.1007/s10571-019-00701-8

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